Like his sister Abby, John III eventually settled on philanthropy as his major interest. His brothers Nelson and Winthrop devoted themselves to politics while Laurance went into conservation and David went into banking. He was a major force behind the establishment of the Council on Foundations, the Foundation Center and Independent Sector. He took a leading role in organizing the Commission on Foundations and Private Philanthropy (better known as the Peterson Commission) and the Commission on Private Philanthropy and Public Needs (better known as the Filer Commission). He also made the initial donation to support Yale University's Program on Non-Profit Organizations, the first academic research center to focus on nonprofits.

Commencing a lifelong commitment to international relations, he undertook a world tour after graduating from college, which concluded with assignments for the Institute of Pacific Relations conference in Japan.[1]

John III was the next Rockefeller manager for all family undertakings of social relevance. Since 1929, in total he sat on twenty boards of various institutions, most of which were family-related. The more notable of these were:

He was a prominent third-generation family philanthropist in his own right and founder of the Asia Society, the major institution he established in 1956 to foster greater cooperation between Asia and the United States. He also founded the Population Council in 1952, and a reconstituted Japan Society. In addition, he set up the United Negro College Fund for the ongoing education of African Americans, carrying on the family tradition in this area with his grandfather's funding of the education of black women at Spelman College in Atlanta.

He was on his father's Advisory Committee in the family office, Room 5600. He was also president of the family's principal philanthropy run by family members, the Rockefeller Brothers Fund, from its inception in 1940 to 1956. In 1929, he joined the family's renowned Rockefeller Foundation; elected to the board in 1931 he subsequently became chairman of this major philanthropic organization for twenty years and was responsible for changing the focus of the institution.

The principal philanthropic institution he created was the JDR III Fund in 1963, its major program being the Asian Cultural Program, created in 1967 to encourage East-West cultural exchange. The Fund was wound-up upon his death in 1979, but the Cultural Program continued as the Asian Cultural Council, which has provided grant assistance to more than 4,000 Asians and Americans in the area of the arts. Funding for its programs is derived from a combination of endowment income and contributions from individuals, foundations and corporations in the United States and Asia.

In the mid-1950s, John III assumed the leadership of a committee of civic leaders who were working to create Lincoln Center. He became the key figure in the fund-raising efforts and in forging a consensus among the civic leaders and others who were essential to its success. The Center itself was built over a period from 1959 to 1966. He was its first president, commencing in 1956, and he became its chairman in 1961. He was chairman until 1970 when he was duly elected honorary chairman.[3]

In the late 1960s, Rockefeller III was responsible for the creation of the Commission on Foundations and Private Philanthropy (usually known as the Peterson Commission, headed by Peter G. Peterson) and the Commission on Private Philanthropy and Public Needs (usually known as the Filer Commission). He established the Rockefeller Public Service Awards in 1958. In 1959, he received The Hundred Year Association of New York's Gold Medal Award "in recognition of outstanding contributions to the City of New York". In 1976, he received the S. Roger Horchow Award for Greatest Public Service by a Private Citizen, an award given out annually by Jefferson Awards.[4]Rockefeller College at Princeton University was named in his honor in 1982.

On November 11, 1932, he married the socially connected Blanchette Ferry Hooker (1909–1992), who was to serve as chairman of the Asian Cultural Council from 1980 to 1990, and who established the Blanchette H. Rockefeller Fellowship Fund, in Japan. They had one son and three daughters:

children of John Davison Rockefeller IIIchildren of Nelson Aldrich Rockefellerchildren of Laurance Spelman Rockefellerchildren of Winthrop Rockefellerchildren of David Rockefellerchildren of Godfrey Stillman Rockefeller